Download article as pdf

Ocular Perfusion Pressure and Pulsatile Ocular
Blood Flow in Normal and Systemic Hypertensive
Patients
ORIGINAL ARTICLE
Sunil Ganekal1, Surendra Shetty1, Syril Dorairaj2
ABSTRACT
Purpose: The purpose was to compare the ocular perfusion pressure (OPP) and the pulsatile ocular blood flow (POBF)
in normal and systemic hypertensive patients.
Materials and Methods: Totally, 121 individuals (normal n = 60, systemic hypertension patients n = 61) were enrolled in
this prospective age-matched comparative study. Intraocular pressure (IOP) and systemic arterial pressure were measured
in seated position with 2 min interval between the measurements using Goldmann applanation tonometer (GAT) and
tycos sphygmomanometer, respectively. The OPP was calculated as 2/3 of mean arterial pressure (MAP) minus IOP.
After 5 min in the seated position POBF measurements were taken with the ocular blood flow (OBF) tonograph.
Results: Mean age was 57.5 years (range 35-72 years) in the normal group and 59.6 years (range 36-78 years) in
the hypertensive group; majority of the patients were female (68.5% and 71% respectively in each group). Measured
parameters in both the groups showed, systolic blood pressure (BP) (143.6 ± 20.5 mmHg vs. 121.9 ± 17.5 mmHg),
diastolic BP (90.7 ± 13.5 mmHg vs. 80.1 ± 9.9 mmHg), MAP (108.4 ± 14.2 mmHg vs. 94.2 ± 11.2 mmHg), and OPP (57.6
± 14.6 vs. 48.7 ± 10.6 mmHg) were significantly greater (P = 0.001) in systemic hypertensive patients in comparison
to normals. However, there was no difference in OBF tonograph values in both groups. The IOP measured by the OBF
tonograph was higher than GAT in both groups, but the difference was not statistically significant (P = 0.41).
Conclusion: Systemic hypertensive patients have a higher OPP in comparison to normal patients, but they do not have
higher POBF. More studies are required to evaluate the role of the OPP in different ocular pathologies affecting the POBF.
KEY WORDS: Ocular perfusion pressure, pulsatile ocular blood flow, systemic hypertension
INTRODUCTION
The fact is that the reduction of the OBF frequently
precedes the structural damage in many eye diseases.[2]
Many techniques exist for the measurement of OBF,
however, there are no techniques available that
provide direct measurement of blood flow in the
eye.[1]
flow have been evaluated with diverse techniques,
including fluorescein angiography, color doppler,
doppler laser flowmetry, and OBF tonograph.[3] It has
been demonstrated that the posterior portion of the
optic nerve is vulnerable to ischemia when the ocular
perfusion pressure (OPP) is reduced.[4] The total OBF
is approximately 1 ml/min.[1] More than 90% of the
total OBF supplies the vasculature of the choroidal
circulation.[5] Since the retinal blood flow accounts
for only 2-5% of the total ocular circulation, it can
be assumed that the pulsatile OBF (POBF) is almost
entirely due to the choroidal circulation.[5]
Blood flow in the eye can be affected by both ocular
and systemic factors.[1] Abnormalities of the blood
The perfusion pressure of ocular vessels is the
difference between intravascular pressure (blood
Measurement of ocular blood flow (OBF) is useful to
study the pathophysiology of several eye diseases as
well as for evaluation of new therapeutic approaches.[1]
Access this article online
Department of Ophthalmology, JJM Medical College,
Davangere, Karnataka, India, 2Department of Ophthalmology,
Mayo Clinic, Jacksonville, Florida 32224, USA
1
Quick Response Code:
Website:
***
Address for correspondence:
Sunil Ganekal, Department of Ophthalmology, JJM Medical College,
Davanagere - 577 004, Karnataka, India. Tel.: 91(8192)-220088,
Fax: 91(8192)-220088, E-mail: [email protected]
Journal of Vision Sciences/Jan-Apr 2015/Volume 1/Issue 1
17
Ganekal, et al.: Ocular perfusion pressure and pulsatile ocular blood flow
pressure [BP]) and intraocular pressure (IOP).[1] The
eye is supplied by the ophthalmic artery in which the
vessel BP is estimated to be 2/3 of the brachial arterial
pressure.[1]
The differences in the responses of the retinal and
choroidal circulation are evident when the OPP is
reduced with the reduction of the choroidal circulation
while the retinal circulation remains stable.[1] Pulsatile
blood flow to the eye induces IOP variations from
which mean pulsatile component of the blood flow
to the eye has been estimated to be approximately
0.724 ml/min.[6]
In agreement with the vascular theory, low systemic
arterial pressure relative to IOP can lead to a low
OPP. On the other hand, systemic hypertension can
increase the risk of damage to the small vessels of the
ocular circulation.[7]
A reduction in mean arterial pressure (MAP) or an
increase in IOP could diminish the ocular perfusion,
but the accurate mechanism of the regulation of
the IOP is still unknown. If the autoregulation
mechanisms are continuous, the sanguineous flow
will remain steady with a substantial fall of the ocular
perfusion.[8]
The pulse of the cardiovascular system is also
expressed in the eye with each systolic-diastolic cycle.
The blood flows in to the ocular blood vessels during
systole and continues to flow more slowly during
diastole. This phenomenon implies a maximum IOP
during systole and a minimum IOP during diastole.
In this way, admitting itself that this relationship is
identical, transitory changes of the IOP allow us to
calculate changes in ocular volume. Pneumatonometric
methods have been used to estimate POBF on the
basis of changes in the measurements of IOP during
the cardiac cycle.[6,9] OBF tonograph is the equipment
sensitive to evaluate minimum changes of the IOP
pulse and to correlate them with volume. However,
it cannot determine the OBF of isolated parts of
the intrinsic vascular net of the eye. Therefore, its
principle is based on the total influx of blood in each
cardiac systole.[9,10] and measures mainly the OBF in
the choroids and anterior portion of the head of the
optic nerve, supplied by the posterior ciliary vessels
that contribute 80-90% of the OBF.[3]
The reduced OBF can have a decisive implication
on the pathophysiology of many ocular illnesses
like diabetic retinopathy, age-related macular
degeneration, pigmentary retinopathy, myopia,
glaucoma, and many of these disorders will have an
association with systemic hypertension. Hence in this
study, our aim was to determine the variations of OPP
and a pulsatile component of total OBF in normal
individuals and persons with systemic hypertension.
MATERIALS AND METHODS
The study was performed in adherence to the
guidelines of the Declaration of Helsinki. The study
protocols were approved by the Ethics Committee
and our Institutional Review Board. Informed consent
was taken from all enrolled patients.
A total of 121 individuals (n = 60 normal and n =
61 newly diagnosed systemic hypertensive) were
enrolled in this prospective age-matched comparative
study and, underwent a complete ophthalmologic
examination including history of systemic
medications, and systemic disease which can affect
the blood flow, previous ocular diseases, trauma or
surgery, slit lamp examination, Goldmann applanation
tonometry (GAT), stereoscopic fundus examination
and OBF tonograph measurements. Both the GAT
and the OBF tonograph were calibrated according to
the manufacturer’s guidelines. Two measurements of
IOP and systemic arterial pressure were taken with
GAT and Tycos sphygmomanometer respectively,
in seated position with 2 min interval between the
measurements. MAP is calculated as 1/3 systolic BP
(SBP) + 2/3 diastolic BP (DBP).[11] Pulse pressure
amplitude is calculated as SBP−DBP.[7] The OPP is
defined as 2/3 of MAP minus IOP (OPP = 2/3 MAP−
IOP).[7,8] After 5 min in the seated position OBF
measurements were taken with the OBF tonograph
(Ocular Blood Flow Laboratories [UK] Ltd.).
Normal patient group included: >35 years of age,
no ocular or systemic diseases, no previous ocular
surgeries, and not on any systemic medications.
Systemic hypertensive patient group included:
>35-year-old, no known ocular pathology or previous
surgeries; diagnosis of hypertension was made, when
the average of 2 or more diastolic BP measurements
on at least 2 subsequent visits was ≥90 mmHg or
when the average of multiple systolic BP readings
Journal of Vision Sciences/Jan-Apr 2015/Volume 1/Issue 1
18
Ganekal, et al.: Ocular perfusion pressure and pulsatile ocular blood flow
on 2 or more subsequent visits is consistently ≥
140 mmHg. Isolated systolic hypertension was
defined as systolic BP ≥ 140 mmHg and diastolic BP
<90 mmHg. In addition, both the groups had patients
with refractive errors between ±6.00D spherical and
±3.00 cylindrical, best corrected visual acuity ≥20/40,
IOP <21 mmHg and cup/disc ratio <0.4 and absence
of cup/disc asymmetry.
The same examiner (SG) took OBF tonograph
measurements in all patients after the instillation of
topical anesthetic eye drop (proparacaine HCl 0.5%).
The OBF tonograph has one pneumotonometer with
disposable tips that is placed against an anesthetized
cornea to measure the IOP pulses. During the
examination, the OBF tonograph produces a sound
that helps the examiner to capture 5 complete IOP
pulses. If after 20 s the equipment is not capable of
detecting 5 complete pulses, the test is automatically
interrupted. The OBF tonograph is capable of detecting
initial tensional levels ranging from 5 mmHg up to
127 mmHg. The data supplied after the detection
of the 5 pulses of the IOP are: IOP, minimum IOP
(in mmHg), pulse amplitude, pulse volume (in µl),
pulse rate (beats/minute) and POBF (µl/min). Only
the right eye’s values were considered for calculation
using the Student’s t-test.
Table 1: Variables of the study
Variables
Normal
Hypertensive
P value
IOP
14.1±3.8
14.7±3.1
0.345
Systolic pressure
121.9±17.5
143.6±20.5
0.001
Diastolic pressure
80.1±9.9
90.7±13.5
0.001
MAP
94.2±11.2
108.4±14.2
0.001
OPP
48.7±10.6
57.6±14.6
0.001
IOP: Intraocular pressure, MAP: Mean arterial pressure, OPP: Ocular
perfusion pressure
Table 2: Descriptive statistic of the POBF tonograph
variability
Hypertensive P value
Variables
Normal
IOP (mmHg)
15.4±3.6
15.3±4.52
0.831
Pulse amplitude (mmHg)
3.6±2.9
3.9±1.92
0.498
Pulse volume (µl)
7.4±2.5
7.4±2.5
0.994
Heart rate (bpm)
77.3±12.7
79.6±16.1
0.505
POBF (µl/min)
20.3±5.7
20.1±5.3
0.895
POBF: Pulsatile ocular blood flow, IOP: Intraocular pressure
RESULTS
Mean age was 57.5 years (range 35-72 years) in
the normal patient group and 59.6 in the systemic
hypertensive group (range 36-78 years). Female
patients were more in both the groups (68.5% and
71%, respectively). SBP (143.6 ± 20.5 mmHg vs.
121.9 ± 17.5 mmHg) and DBP (90.7 ± 13.5 mmHg
vs. 80.1 ± 9.9 mmHg), MAP (108.4 ± 14.2 mmHg vs.
94.2 ± 11.2 mmHg) and OPP (57.6 ± 14.6 vs. 48.7 ±
10.6 mmHg) were significantly greater in the systemic
hypertensive patients in comparison to normals
(Figure 1 and Table 1). There was no difference in
all OBF tonograph values in both groups (Table 2).
The IOP measured by the OBF tonograph was higher
than GAT in both groups, but the difference was not
statistically significant (P = 0.41).
DISCUSSION
Previous studies consider the normal IOP to be
between 10 and 20 mmHg.[12]
Figure 1: Comparison of the ocular perfusion pressure of normal
and systemic hypertensive patients in mmHg (P = 0.001)
In this study, the mean IOP was 14.5 mmHg (standard
deviation [SD] 3.5), with no significant difference
between the groups and higher with the OBF
tonograph. Confirming the good division of the groups,
the MAP in our normal patients was 94.2 mmHg (SD
11.2), while in the systemic hypertensive patients was
108.4 mmHg (SD 14.78).
Leske et al. investigating the relationship between
OPP and incidence of open-angle glaucoma
reported a relative risk of 3.1 for patients with OPP
<41.0 mmHg.[7] Our results have demonstrated an
OPP of 48.7 mmHg (SD 10.6) in normal patients and
of 53.5 mmHg (SD 14.6) in systemic hypertensive
Journal of Vision Sciences/Jan-Apr 2015/Volume 1/Issue 1
19
Ganekal, et al.: Ocular perfusion pressure and pulsatile ocular blood flow
patients. This significant difference (P = 0.001)
confirms a higher OPP in the systemic hypertensive
patients.
Grunwald et al.[13] reported that glaucoma patients
with systemic hypertension had higher optic nerve
blood flow and may help to maintain adequate
perfusion of the optic nerve. According to our
results, although systemic hypertensive patients
had greater OPP, they did not have greater POBF
values measured by the OBF tonographsimilar to the
findings of Niknam et al.[14] who used laser Doppler
flowmetry.
There is evidence of an abnormal association
between ocular perfusion parameters and systemic
BP. However, these data refer to the long-term
perfusion adaptation of the eye to BP rather than
a short-term increase in BP.[15] Despite this, we
cannot quantify with any current diagnostic method
the real amount of blood in the anterior portion of
the optic nerve, nor the level of existing gaseous
exchange in this place. We also do not have a reliable
technique to measure the blood flow in the anterior
portion of the optic nerve. It is important to point
out that although systemic arterial hypertensive
patients have a better ocular OPP in comparison
to the normal population, they do not necessarily
have a better ocular nutrition, because of significant
vascular alterations.[16]
Yang et al.[17] reported average POBF values of 11.16
µl/s for men and 14.03 µl/s for women, and suggested
that this difference was a consequence of the faster
cardiac frequency in the women. In another study,
Massey and Crowhurst, found POBF values of 13.46
µl/s with women having greater POBF values. Myopia,
increase of the IOP, and older age are related to reduced
POBF values.[18] Our study showed POBF values were
20.31 µl/s (SD 0.98) in normal patients and 20.15 µl/s
(SD 0.75) in systemic hypertensive patients. This
difference was not statistically significant (P = 0.895).
The variability of the OBF tonograph measurements
has been attributed to a great number of variables,
e.g. age, sex, cardiac frequency, pregnancy, body
position, and ocular axial diameter.[3] Although we
observed a significant difference in systemic arterial
pressure among normal and hypertensive patients they
had close POBF readings suggesting the existence of
intrinsic factors related to the ocular hemodynamics or
extrinsic factors related to the device or its software that
regulates the OBF or makes its measurement complex.
In summary, although the systemic hypertensive
patients have a higher OPP in comparison to normal
patients they do not have higher OBF. More studies
are required to evaluate the role of the OPP and
changes in POBF in various eye disorders.
REFERENCES
1. Williamson TH, Harris A. Ocular blood flow measurement.
Br J Ophthalmol 1994;78:939-45.
2. Flammer J, Orgül S, Costa VP, Orzalesi N, Krieglstein GK,
Serra LM, et al. The impact of ocular blood flow in
glaucoma. Prog Retin Eye Res 2002;21:359-93.
3. Aydin A, Wollstein G, Price LL, Schuman JS. Evaluating
pulsatile ocular blood flow analysis in normal and treated
glaucomatous eyes. Am J Ophthalmol 2003;136:448-53.
4. Hayreh SS. Blood supply of the optic nerve head: A
“reality check”. In: Pullunat LE, Harris A, Anderson DR,
Greve EL, editors. Current Concepts on Ocular Blood Flow
in Glaucoma. New York: Kugler; 1999. p. 3-31.
5. Hill DW. Measurement of retinal blood flow. Trans
Ophthalmol Soc UK 1976;96:199-201.
6. Langham ME, Farrell RA, O’Brien V, Silver DM,
Schilder P. Blood flow in the human eye. Acta Ophthalmol
Suppl 1989;191:9-13.
7. Leske MC, Wu SY, Nemesure B, Hennis A. Incident openangle glaucoma and blood pressure. Arch Ophthalmol
2002;120:954-9.
8. Singleton CD, Robertson D, Byrne DW, Joos KM. Effect
of posture on blood and intraocular pressures in multiple
system atrophy, pure autonomic failure, and baroreflex
failure. Circulation 2003;108:2349-54.
9. Silver DM, Farrell RA, Langham ME, O’Brien V, Schilder
P. Estimation of pulsatile ocular blood flow from intraocular
pressure. Acta Ophthalmol Suppl 1989;191:25-9.
10. James CB. Pulsatile ocular blood flow. Br J Ophthalmol
1998;82:720-1.
11. Aim A, Bill A. Ocular circulation. In: Hart WW, editor.
Alder’s Physiology of the Eye. St. Louis: Mosby; 1987. p.
183-203.
12. Fuchsjäger-Mayrl G, Wally B, Georgopoulos M, Rainer G,
Kircher K, Buehl W, et al. Ocular blood flow and systemic
blood pressure in patients with primary open-angle
glaucoma and ocular hypertension. Invest Ophthalmol Vis
Sci 2004;45:834-9.
13. Grunwald JE, Piltz J, Hariprasad SM, DuPont J. Optic nerve
and choroidal circulation in glaucoma. Invest Ophthalmol
Vis Sci 1998;39:2329-36.
14. Niknam RM, Schocket LS, Metelitsina T, DuPont JC,
Grunwald JE. Effect of hypertension on foveolar choroidal
haemodynamics. Br J Ophthalmol 2004;88:1263-5.
Journal of Vision Sciences/Jan-Apr 2015/Volume 1/Issue 1
20
Ganekal, et al.: Ocular perfusion pressure and pulsatile ocular blood flow
15. Sehi M, Flanagan JG, Zeng L, Cook RJ, Trope GE. Relative
change in diurnal mean ocular perfusion pressure: a risk
factor for the diagnosis of primary open-angle glaucoma.
Invest Ophthalmol Vis Sci 2005;46:561-7.
16. Weigert G, Findl O, Luksch A, Rainer G, Kiss B, Vass C,
et al. Effects of moderate changes in intraocular pressure
on ocular hemodynamics in patients with primary openangle glaucoma and healthy controls. Ophthalmology
2005;112:1337-42.
17.Yang YC, Hulbert MF, Batterbury M, Clearkin LG.
Pulsatile ocular blood flow measurements in healthy
eyes: reproducibility and reference values. J Glaucoma
1997;6:175-9.
18. Massey AD, O’Brien C, Crowhurst C. Pulsatile ocular blood
flow: A population study of normals. Invest Ophthal Vis Sci
1996;37:S31.
How to cite this article: Ganekal S, Shetty S, Dorairaj S.
Ocular Perfusion Pressure and Pulsatile Ocular Blood Flow
in Normal and Systemic Hypertensive Patients. J Vis Sci
2015;1(1):17-21.
Financial Support: None; Conflict of Interest: None
Journal of Vision Sciences/Jan-Apr 2015/Volume 1/Issue 1
21